Segregation of Lolium perenne into a subpopulation with high infection by endophyte Epichloë festucae var. lolii results in improved agronomic performance
Background and aims
Low temperature stress is a common hazard during plant growth. Endophyte infection has been shown to increase cold tolerance in host plants. Many Lolium perenne cultivars contain low to moderate levels of endophyte. This study was done to explore cultivar improvement by segregation of endophyte containing individuals from the original cultivar to create a high endophyte subpopulation.
Endophyte-infected plants were segregated over the first 3 years to produce high-endophyte subpopulation, and field and greenhouse experiments were carried out in the forth and fifth to determine the cold tolerance of the L. perenne subpopulation with high endophyte infection rates (N), the parent (F), the control endophyte-free subpopulation (E) and the control local variety (L).
(1) After 3 years of screening, high endophyte infection rates in the tillers and seeds of plants were still observed (96.5%), and agronomic traits (crown width, plant height, panicle number, withering, regreen-up, the growth cycle and the over-wintering rate) was also improved with increased Epichloë colonization of host plant. (2) The subpopulation with high endophyte infection rates and improved agronomic traits had better cold tolerance than the parent, the control endophyte-free subpopulation and the control local variety. The possible mechanisms by which high endophyte infection enhances cold resistance in the field include increased root system, increased the over-wintering rate, reduced regrowth periods with the sowing date being October 15th. (3) The high-endophyte subpopulation significantly increased SOD, POD, CAT, and APX activities at 0, 5, and 10 °C by 11.8%–44.6%, compared with the parent population.
The subpopulation had a high endophyte infection rate, improved agronomic traits and higher enzymatic activities. These results indicate that increasing endophyte infection rates by selection, effectively improved agronomic traits and cold tolerance.
KeywordsLolium perenne E. festucae var. lolii Endophyte infection rate Cold tolerance Sowing date Low temperature stress
We thank Jingle Zhou, Jing Liu, Hao Chen, and Weihu Lin for help with this experiments, and Taixiang Chen and Xiang Yao for beneficial discussions regarding the manuscript.
This research was supported by the National Basic Research Program of China (2014CB138702), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0302), the Strategic Priority Research Program of Chinese Academy of Sciences (XDA20100102), Program for Changjiang Scholars and Innovative Research Team in University, China (IRT17R50), Fundamental Research Funds for the Central Universities (LZUJBKY-2018-kb10 and 2019-kb10) and 111 Project (B12002). The authors are thankful for support from USDA-NIFA Multistate Project W4147, and the New Jersey Agricultural Experiment Station.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interests.
- Barnawal D, Bharti N, Tripathi A, Pandey SS, Chanotiya CS, Kalra A (2016) ACC-deaminase-producing endophyte brachybacterium paraconglomeratum strain SMR20 ameliorates chlorophytum salinity stress via altering phytohormone generation. J Plant Growth Regul 35:1–12. https://doi.org/10.1007/s00344-015-9560-3 CrossRefGoogle Scholar
- Barrero-Gil J, Huertas R, Rambla JL, Granell A, Salinas J (2016) Tomato plants increase their tolerance to low temperature in a chilling acclimation process entailing comprehensive transcriptional and metabolic adjustments. Plant Cell Environ 39:2303–2318. https://doi.org/10.1111/pce.12799 CrossRefPubMedGoogle Scholar
- Chen N (2008) Genetic diversity of drunken horse grass (Achnatherum inebrians) and effects of its endophyte infection on cold tolerance. Thesis (Ph.D.): LanZhou University. (In Chinese, with English abstract)Google Scholar
- Chen Y, Jiang JF, Chang QC, Gu CS, Song AP, Chen SM, Dong B, Chen FD (2014) Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol Biol Rep 41:815–822. https://doi.org/10.1007/s11033-013-2921-8 CrossRefPubMedGoogle Scholar
- Chen N, He RL, Chai Q, Li CJ, Nan ZB (2016) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regul 80:367–375. https://doi.org/10.1007/s10725-016-0177-8 CrossRefGoogle Scholar
- Chen ZJ, Wei XK, Ying C, Tian P, Zhao XJ, Li CJ (2017) Research progress of methods on grass fungal endophyte detection. Pratacult Sci 11:1419–1433 (In Chinese, with English abstract)Google Scholar
- Chen ZJ, Chen H, Wei XK, Tian P, Li CJ, Nan ZB (2018b) Screening of individual plants of Lolium perenne with high endophyte infection rate.10th International Symposium on Fungal Endophytes of Grasses: Book of abstracts 77. http://isfeg2018.fundacionusal.es/
- Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics Biology Fg B 45:84–93. https://doi.org/10.1016/j.fgb.2007.07.013 CrossRefPubMedGoogle Scholar
- Dalmannsdottir S, Jørgensen M, Rapacz M, Østrem L, Larsen A, Rødven R, Rognli OA (2017) Cold acclimation in warmer extended autumns impairs freezing tolerance of perennial ryegrass (Lolium perenne) and timothy (Phleum pratense). Physiol Plant 160:266–281. https://doi.org/10.1111/ppl.12548 CrossRefPubMedGoogle Scholar
- Han H, Han B (2015) Evaluation of cold resistance and selection of chill-proof measure of three Phlox cultivars. J Anim Plant Sci 25:208–212Google Scholar
- Hennessy LM, Popay AJ, Finch SC, Clearwater MJ, Cave VM (2016) Temperature and plant genotype alter alkaloid concentrations in ryegrass infected with an Epichloë endophyte and this affects an insect herbivore. Front Plant Sci 7:1907–1917. https://doi.org/10.3389/fpls.2016.01097 CrossRefGoogle Scholar
- Hill NS, Stringer WC, Rottinghaus GE, Belesky DP, Parrott WA, Pope DD (1990) Growth, morphological and chemical component responses of tall fescue to Acremonium coenophialum. Crop Sci 30:239–255 https://www.crops.org/publications cs/abstracts/30/1/CS0300010156 CrossRefGoogle Scholar
- Hume DE, Cooper BM, Panckhurst KA (2009) The role of endophyte in determining the persistence and productivity of ryegrass, tall fescue and meadow fescue in Northland. Proc N Z Grassl Assoc 71:145–150Google Scholar
- Kong LY, Yan H, Bao YS, Chen HL (2012) Remote sensor monitoring method for winter wheat growth based on key development periods. Chin J Agrometeorol 33:424–430 (In Chinese, with English abstract)Google Scholar
- Kovi MR, Fjellheim S, Sandve SR, Larsen A, Rudi H, Asp T, Kent MP, Rognli OA (2015) Population structure, genetic variation, and linkage disequilibrium in perennial ryegrass populations divergently selected for freezing tolerance. Front Plant Sci 6:929–942. https://doi.org/10.3389/fpls.2015.00929 CrossRefPubMedPubMedCentralGoogle Scholar
- Ma MZ, Christensen MJ, Nan ZB (2015) Effects of the endophyte Epichloë festucae var. lolii of perennial ryegrass (Lolium perenne) on indicators of oxidative stress from pathogenic fungi during seed germination and seedling growth. Eur J Plant Pathol 141:571–583. https://doi.org/10.1007/s10658-014-0563-x CrossRefGoogle Scholar
- Maejima A, Saiga S, Inoue T, Tsuiki M (2000) Endophyte infection rate and alkaloid concentrations in seeds of commercial cultivars of perennial ryegrass. Jap J Grassl Sci 46:52–57Google Scholar
- Mohammadian MA, Largani ZK, Sajedi RH (2012) Quantitative and qualitative comparison of antioxidant activity in the flavedo tissue of three cultivars of citrus fruit under cold stress. Aust J Crop Sci 6:402–406Google Scholar
- Narra S (2007) Evaluation of sensing and machine vision techniques in stress detection and quality evaluation of turfgrass species. Thesis (Ph.D.): University of Illinois at Urbana-Champaign. http://hdl.handle.net/2142/83121
- Orabi SA, Salman SR, Shalaby MAF (2010) Increasing resistance to oxidative damage in cucumber (Cucumis sativus L.) plants by exogenous application of salicylic acid and paclobutrazol. World J Agric Sci 6:252–259Google Scholar
- Qawasmeh A, Obied HK, Raman A, Wheatley W (2012) Influence of fungal endophyte infection on phenolic content and antioxidant activity in grasses: Interaction between Lolium perenne and different srains of Neotyphodium lolii. J Agric Food Chem 60:3381–3388. https://doi.org/10.1021/jf204105k CrossRefPubMedGoogle Scholar
- Redman RS, Yong OK, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:e14823–e14833. https://doi.org/10.1371/journal.pone.0014823 CrossRefPubMedPubMedCentralGoogle Scholar
- Sanghera GS, Wani SH, Wasim H, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12:30–43. http://www.ncbi.nlm.nih.gov/pmc/articles/. PMC 3129041
- Scebba F, Sebastiani L, Vitagliano C (1998) Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiol Plant 104:747–752. https://doi.org/10.1034/j.1399-3054.1998.1040433.x CrossRefGoogle Scholar
- Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal wendophytes. Annu Rev Plant Biol 55:315–340. https://doi.org/10.1146/annurev.arplant.55.031903.141735 CrossRefPubMedGoogle Scholar
- Wheatley WM, Kemp HW, Simpson WR, Hume DE, Nicol HI, Kemp DR, Launders TE (2007) Viability of endemic endophyte (Neotyphodium lolii) and perennial ryegrass (Lolium perenne) seed at retail and wholesale outlets in south-eastern Australia. Seed Sci Technol 35:360–370. https://doi.org/10.15258/sst.2007.35.2.11 CrossRefGoogle Scholar
- White JF, Sullivan RF, Moy M, Meyer W, Cabral D (2001) Evolution of Epichloë/ Neotyphodium endophytes and other clavicipitalean biotrophs. Symbiosis: Mechanisms and Model Systems (Cellular Origin, Life in Extreme Habitats and Astrobiology). https://doi.org/10.1007/0-306-48173-1_26
- Zhang XQ, Huang GQ, Huang ZL, Bian XM, Jiang XH (2012) Effects of low temperature on freezing injury of various winter wheat cultivars at different sowing time. Agric Sci Technol: English Edn 13:2332–2337Google Scholar
- Zhang T, Zhang YQ, Liu HY, Wei YZ, Li HL, Su J, Zhao LX, Yu LY (2013) Diversity and cold adaptation of culturable endophytic fungi from bryophytes in the Fildes Region, King George Island, maritime Antarctica. FEMS Microbiol Lett 341:52–61. https://doi.org/10.1111/1574-6968.12090 CrossRefPubMedGoogle Scholar